Current Cardiology Reports

, 21:90 | Cite as

Bioprinting Approaches to Engineering Vascularized 3D Cardiac Tissues

  • Nazan Puluca
  • Soah Lee
  • Stefanie Doppler
  • Andrea Münsterer
  • Martina Dreßen
  • Markus Krane
  • Sean M. WuEmail author
Regenerative Medicine (SM Wu, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Regenerative Medicine


Purpose of Review

3D bioprinting technologies hold significant promise for the generation of engineered cardiac tissue and translational applications in medicine. To generate a clinically relevant sized tissue, the provisioning of a perfusable vascular network that provides nutrients to cells in the tissue is a major challenge. This review summarizes the recent vascularization strategies for engineering 3D cardiac tissues.

Recent Findings

Considerable steps towards the generation of macroscopic sizes for engineered cardiac tissue with efficient vascular networks have been made within the past few years. Achieving a compact tissue with enough cardiomyocytes to provide functionality remains a challenging task. Achieving perfusion in engineered constructs with media that contain oxygen and nutrients at a clinically relevant tissue sizes remains the next frontier in tissue engineering.


The provisioning of a functional vasculature is necessary for maintaining a high cell viability and functionality in engineered cardiac tissues. Several recent studies have shown the ability to generate tissues up to a centimeter scale with a perfusable vascular network. Future challenges include improving cell density and tissue size. This requires the close collaboration of a multidisciplinary teams of investigators to overcome complex challenges in order to achieve success.


3D printing Cardiac engineered tissue Vascularization Bioprinting Cardiovascular tissue Cardiomyocyte 



We thank Mark Skylar-Scott, PhD (Wyss Institute for Biologically Inspired Engineering, Harvard University) for his comments and edits on the manuscript.


Funding for this research was provided by the German Research Foundation/DFG (PU 690/1-1) (N.P.), the NIH Office of Director’s Pioneer Award LM012179-03, the American Heart Association Established Investigator Award 17EIA33410923, the Stanford Cardiovascular Institute, the Hoffmann and Schroepfer Foundation, and the Stanford Division of Cardiovascular Medicine, Department of Medicine (S.M.W). The authors declare no other relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript apart from those disclosed. No writing assistance was utilized in the production of this manuscript.

Compliance with Ethical Standards

Conflict of Interest

Nazan Puluca, Soah Lee, Stephanie Doppler, Andrea Münsterer, Martina Dreßen, Markus Krane, and Sean M. Wu declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.


Papers of particular interest, published recently, have been highlighted as: •• Of major importance

  1. 1.
    Lopez AD, Mathers CD, Ezzati M, Jamison DT, Murray CJL. Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. Lancet Lond Engl. 2006;367(9524):1747–57.Google Scholar
  2. 2.
    Benjamin EJ, Muntner P, Alonso A, Bittencourt MS, Callaway CW, Carson AP, et al. Heart Disease and Stroke Statistics-2019 update: a report from the American Heart Association. Circulation. 2019;31:CIR0000000000000659.Google Scholar
  3. 3.
    Chambers DC, Cherikh WS, Goldfarb SB, Hayes D, Kucheryavaya AY, Toll AE, et al. The International Thoracic Organ Transplant Registry of the International Society for Heart and Lung Transplantation: thirty-fifth adult lung and heart-lung transplant report-2018; focus theme: multiorgan transplantation. J Heart Lung Transplant Off Publ Int Soc Heart Transplant. 2018;37(10):1169–83.Google Scholar
  4. 4.
    Zhang YS, Aleman J, Arneri A, Bersini S, Piraino F, Shin SR, et al. From cardiac tissue engineering to heart-on-a-chip: beating challenges. Biomed Mater Bristol Engl. 2015;10(3):034006.Google Scholar
  5. 5.
    Vunjak-Novakovic G, Tandon N, Godier A, Maidhof R, Marsano A, Martens TP, et al. Challenges in cardiac tissue engineering. Tissue Eng Part B Rev. 2010;16(2):169–87.PubMedGoogle Scholar
  6. 6.
    Bergmann O, Bhardwaj RD, Bernard S, Zdunek S, Barnabé-Heider F, Walsh S, et al. Evidence for cardiomyocyte renewal in humans. Science. 2009;324(5923):98–102.PubMedPubMedCentralGoogle Scholar
  7. 7.
    Kajstura J, Gurusamy N, Ogórek B, Goichberg P, Clavo-Rondon C, Hosoda T, et al. Myocyte turnover in the aging human heart. Circ Res. 2010;107(11):1374–86.PubMedGoogle Scholar
  8. 8.
    Burridge PW, Matsa E, Shukla P, Lin ZC, Churko JM, Ebert AD, et al. Chemically defined generation of human cardiomyocytes. Nat Methods. 2014;11(8):855–60.PubMedPubMedCentralGoogle Scholar
  9. 9.
    Zhang J, Wilson GF, Soerens AG, Koonce CH, Yu J, Palecek SP, et al. Functional cardiomyocytes derived from human induced pluripotent stem cells. Circ Res. 2009;104(4):e30–41.PubMedPubMedCentralGoogle Scholar
  10. 10.
    Derakhshanfar S, Mbeleck R, Xu K, Zhang X, Zhong W, Xing M. 3D bioprinting for biomedical devices and tissue engineering: a review of recent trends and advances. Bioact Mater. 2018;3(2):144–56.PubMedPubMedCentralGoogle Scholar
  11. 11.
    Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol. 2014;32(8):773–85.PubMedGoogle Scholar
  12. 12.
    Ubil E, Duan J, Pillai ICL, Rosa-Garrido M, Wu Y, Bargiacchi F, et al. Mesenchymal-endothelial transition contributes to cardiac neovascularization. Nature. 2014;514(7524):585–90.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Sun X, Altalhi W, Nunes SS. Vascularization strategies of engineered tissues and their application in cardiac regeneration. Adv Drug Deliv Rev. 2016;96:183–94.PubMedGoogle Scholar
  14. 14.
    Ali M, Pages E, Ducom A, Fontaine A, Guillemot F. Controlling laser-induced jet formation for bioprinting mesenchymal stem cells with high viability and high resolution. Biofabrication. 2014;6(4):045001.PubMedGoogle Scholar
  15. 15.
    Billiet T, Vandenhaute M, Schelfhout J, Van Vlierberghe S, Dubruel P. A review of trends and limitations in hydrogel-rapid prototyping for tissue engineering. Biomaterials. 2012;33(26):6020–41.PubMedGoogle Scholar
  16. 16.
    Gao G, Schilling AF, Hubbell K, Yonezawa T, Truong D, Hong Y, et al. Improved properties of bone and cartilage tissue from 3D inkjet-bioprinted human mesenchymal stem cells by simultaneous deposition and photocrosslinking in PEG-GelMA. Biotechnol Lett. 2015;37(11):2349–55.PubMedGoogle Scholar
  17. 17.
    Ning L, Chen X. A brief review of extrusion-based tissue scaffold bio-printing. Biotechnol J. 2017;12(8).Google Scholar
  18. 18.
    Gou M, Qu X, Zhu W, Xiang M, Yang J, Zhang K, et al. Bio-inspired detoxification using 3D-printed hydrogel nanocomposites. Nat Commun. 2014;5:3774.PubMedPubMedCentralGoogle Scholar
  19. 19.
    Serpooshan V, Mahmoudi M, Hu DA, Hu JB, Wu SM. Bioengineering cardiac constructs using 3D printing. J 3D Print Med. 2017;1(2):123–39.Google Scholar
  20. 20.
    Hopp B. Femtosecond laser printing of living cells using absorbing film-assisted laser-induced forward transfer. Opt Eng. 2012;51(1):014302.Google Scholar
  21. 21.
    Guillotin B, Souquet A, Catros S, Duocastella M, Pippenger B, Bellance S, et al. Laser assisted bioprinting of engineered tissue with high cell density and microscale organization. Biomaterials. 2010;31(28):7250–6.PubMedGoogle Scholar
  22. 22.
    Nahmias Y, Schwartz RE, Verfaillie CM, Odde DJ. Laser-guided direct writing for three-dimensional tissue engineering. Biotechnol Bioeng. 2005;92(2):129–36.PubMedGoogle Scholar
  23. 23.
    Hölzl K, Lin S, Tytgat L, Van Vlierberghe S, Gu L, Ovsianikov A. Bioink properties before, during and after 3D bioprinting. Biofabrication. 2016;23;8(3):032002.Google Scholar
  24. 24.
    Xu T, Baicu C, Aho M, Zile M, Boland T. Fabrication and characterization of bio-engineered cardiac pseudo tissues. Biofabrication. 2009;1(3):035001.PubMedPubMedCentralGoogle Scholar
  25. 25.
    Gruene M, Deiwick A, Koch L, Schlie S, Unger C, Hofmann N, et al. Laser printing of stem cells for biofabrication of scaffold-free autologous grafts. Tissue Eng Part C Methods. 2011;17(1):79–87.PubMedGoogle Scholar
  26. 26.
    Calvert P. MATERIALS SCIENCE: printing cells. Science. 2007;318(5848):208–9.PubMedGoogle Scholar
  27. 27.
    Cui X, Boland T. Human microvasculature fabrication using thermal inkjet printing technology. Biomaterials. 2009;30(31):6221–7.PubMedGoogle Scholar
  28. 28.
    Chang CC, Boland ED, Williams SK, Hoying JB. Direct-write bioprinting three-dimensional biohybrid systems for future regenerative therapies. J Biomed Mater Res B Appl Biomater. 2011;98(1):160–70.PubMedPubMedCentralGoogle Scholar
  29. 29.
    Okamoto T, Suzuki T, Yamamoto N. Microarray fabrication with covalent attachment of DNA using bubble jet technology. Nat Biotechnol. 2000;18(4):438–41.PubMedGoogle Scholar
  30. 30.
    Goldmann T, Gonzalez JS. DNA-printing: utilization of a standard inkjet printer for the transfer of nucleic acids to solid supports. J Biochem Biophys Methods. 2000;42(3):105–10.PubMedGoogle Scholar
  31. 31.
    Saunders RE, Gough JE, Derby B. Delivery of human fibroblast cells by piezoelectric drop-on-demand inkjet printing. Biomaterials. 2008;29(2):193–203.PubMedGoogle Scholar
  32. 32.
    Cui X, Boland T, D’Lima DD, Lotz MK. Thermal inkjet printing in tissue engineering and regenerative medicine. Recent Pat Drug Deliv Formul. 2012;6(2):149–55.PubMedPubMedCentralGoogle Scholar
  33. 33.
    Pati F, Jang J, Ha D-H, Won Kim S, Rhie J-W, Shim J-H, et al. Printing three-dimensional tissue analogues with decellularized extracellular matrix bioink. Nat Commun. 2014;5:3935.PubMedPubMedCentralGoogle Scholar
  34. 34.
    Mironov V, Visconti RP, Kasyanov V, Forgacs G, Drake CJ, Markwald RR. Organ printing: tissue spheroids as building blocks. Biomaterials. 2009;30(12):2164–74.PubMedPubMedCentralGoogle Scholar
  35. 35.
    Kim JD, Choi JS, Kim BS, Chan Choi Y, Cho YW. Piezoelectric inkjet printing of polymers: stem cell patterning on polymer substrates. Polymer. 2010;51(10):2147–54.Google Scholar
  36. 36.
    Murphy SV, Skardal A, Atala A. Evaluation of hydrogels for bio-printing applications. J Biomed Mater Res A. 2013;101(1):272–84.PubMedGoogle Scholar
  37. 37.
    Khalil S, Sun W. Biopolymer deposition for freeform fabrication of hydrogel tissue constructs. Mater Sci Eng C. 2007;27(3):469–78.Google Scholar
  38. 38.
    Hennink WE, van Nostrum CF. Novel crosslinking methods to design hydrogels. Adv Drug Deliv Rev. 2002;54(1):13–36.PubMedGoogle Scholar
  39. 39.
    Turksen K. Bioprinting in regenerative medicine. Cham Heidelberg New York: Springer; 2015. 140 p. (Stem cell biology and regenerative medicine)Google Scholar
  40. 40.
    Ozbolat IT, Hospodiuk M. Current advances and future perspectives in extrusion-based bioprinting. Biomaterials. 2016;76:321–43.PubMedGoogle Scholar
  41. 41.
    Chang R, Nam J, Sun W. Effects of dispensing pressure and nozzle diameter on cell survival from solid freeform fabrication-based direct cell writing. Tissue Eng Part A. 2008;14(1):41–8.PubMedGoogle Scholar
  42. 42.
    Jones N. Science in three dimensions: the print revolution. Nature. 2012;487(7405):22–3.PubMedGoogle Scholar
  43. 43.
    •• Kolesky DB, Homan KA, Skylar-Scott MA, Lewis JA. Three-dimensional bioprinting of thick vascularized tissues. Proc Natl Acad Sci U S A. 2016;113(12):3179–84. This manuscript shows pioneering work creating thick perfusable tissue.PubMedPubMedCentralGoogle Scholar
  44. 44.
    Irvine SA, Agrawal A, Lee BH, Chua HY, Low KY, Lau BC, et al. Printing cell-laden gelatin constructs by free-form fabrication and enzymatic protein crosslinking. Biomed Microdevices. 2015;17(1):16.PubMedPubMedCentralGoogle Scholar
  45. 45.
    Laronda MM, Rutz AL, Xiao S, Whelan KA, Duncan FE, Roth EW, et al. A bioprosthetic ovary created using 3D printed microporous scaffolds restores ovarian function in sterilized mice. Nat Commun. 2017;16;8:15261.Google Scholar
  46. 46.
    Gao G, Yonezawa T, Hubbell K, Dai G, Cui X. Inkjet-bioprinted acrylated peptides and PEG hydrogel with human mesenchymal stem cells promote robust bone and cartilage formation with minimal printhead clogging. Biotechnol J. 2015;10(10):1568–77.PubMedGoogle Scholar
  47. 47.
    Schiele NR, Corr DT, Huang Y, Raof NA, Xie Y, Chrisey DB. Laser-based direct-write techniques for cell printing. Biofabrication. 2010;2(3):032001.PubMedPubMedCentralGoogle Scholar
  48. 48.
    Duan B, Hockaday LA, Kang KH, Butcher JT. 3D bioprinting of heterogeneous aortic valve conduits with alginate/gelatin hydrogels. J Biomed Mater Res A. 2013;101(5):1255–64.PubMedGoogle Scholar
  49. 49.
    Ozbolat IT, Yu Y. Bioprinting toward organ fabrication: challenges and future trends. IEEE Trans Biomed Eng. 2013;60(3):691–9.PubMedGoogle Scholar
  50. 50.
    Panwar A, Tan LP. Current status of bioinks for micro-extrusion-based 3D bioprinting. Mol Basel Switz. 2016;25:21(6).Google Scholar
  51. 51.
    Chimene D, Lennox KK, Kaunas RR, Gaharwar AK. Advanced bioinks for 3D printing: a materials science perspective. Ann Biomed Eng. 2016;44(6):2090–102.PubMedGoogle Scholar
  52. 52.
    Gopinathan J, Noh I. Recent trends in bioinks for 3D printing. Biomater Res [Internet]. 2018 Dec [cited 2019 Feb 28];22(1). Available from:
  53. 53.
    Tirella A, Orsini A, Vozzi G, Ahluwalia A. A phase diagram for microfabrication of geometrically controlled hydrogel scaffolds. Biofabrication. 2009;1(4):045002.PubMedGoogle Scholar
  54. 54.
    Gudapati H, Dey M, Ozbolat I. A comprehensive review on droplet-based bioprinting: past, present and future. Biomaterials. 2016;102:20–42.PubMedGoogle Scholar
  55. 55.
    Li S, Xiong Z, Wang X, Yan Y, Liu H, Zhang R. Direct fabrication of a hybrid cell/hydrogel construct by a double-nozzle assembling technology. J Bioact Compat Polym. 2009;24(3):249–65.Google Scholar
  56. 56.
    Gaetani R, Feyen DAM, Verhage V, Slaats R, Messina E, Christman KL, et al. Epicardial application of cardiac progenitor cells in a 3D-printed gelatin/hyaluronic acid patch preserves cardiac function after myocardial infarction. Biomaterials. 2015;61:339–48.PubMedGoogle Scholar
  57. 57.
    Duan B, Kapetanovic E, Hockaday LA, Butcher JT. Three-dimensional printed trileaflet valve conduits using biological hydrogels and human valve interstitial cells. Acta Biomater. 2014;10(5):1836–46.PubMedGoogle Scholar
  58. 58.
    Censi R, van Putten S, Vermonden T, di Martino P, van Nostrum CF, Harmsen MC, et al. The tissue response to photopolymerized PEG-p (HPMAm-lactate)-based hydrogels. J Biomed Mater Res A. 2011;97(3):219–29.PubMedGoogle Scholar
  59. 59.
    Schuurman W, Levett PA, Pot MW, van Weeren PR, Dhert WJA, Hutmacher DW, et al. Gelatin-methacrylamide hydrogels as potential biomaterials for fabrication of tissue-engineered cartilage constructs. Macromol Biosci. 2013;13(5):551–61.PubMedGoogle Scholar
  60. 60.
    Stanton MM, Samitier J, Sánchez S. Bioprinting of 3D hydrogels. Lab Chip. 2015;15(15):3111–5.PubMedGoogle Scholar
  61. 61.
    Hoffman AS. Hydrogels for biomedical applications. Adv Drug Deliv Rev. 2002;54(1):3–12.PubMedGoogle Scholar
  62. 62.
    Jose RR, Rodriguez MJ, Dixon TA, Omenetto F, Kaplan DL. Evolution of bioinks and additive manufacturing technologies for 3D bioprinting. ACS Biomater Sci Eng. 2016;2(10):1662–78.Google Scholar
  63. 63.
    Wang Z, Abdulla R, Parker B, Samanipour R, Ghosh S, Kim K. A simple and high-resolution stereolithography-based 3D bioprinting system using visible light crosslinkable bioinks. Biofabrication. 2015;7(4):045009.PubMedGoogle Scholar
  64. 64.
    Christensen K, Xu C, Chai W, Zhang Z, Fu J, Huang Y. Freeform inkjet printing of cellular structures with bifurcations. Biotechnol Bioeng. 2015;112(5):1047–55.PubMedGoogle Scholar
  65. 65.
    Müller M, Becher J, Schnabelrauch M, Zenobi-Wong M. Nanostructured Pluronic hydrogels as bioinks for 3D bioprinting. Biofabrication. 2015;7(3):035006.PubMedGoogle Scholar
  66. 66.
    Ruan J-L, Tulloch NL, Razumova MV, Saiget M, Muskheli V, Pabon L, et al. Mechanical stress conditioning and electrical stimulation promote contractility and force maturation of induced pluripotent stem cell-derived human cardiac tissue. Circulation. 2016;134(20):1557–67.PubMedPubMedCentralGoogle Scholar
  67. 67.
    Radisic M, Park H, Shing H, Consi T, Schoen FJ, Langer R, et al. Functional assembly of engineered myocardium by electrical stimulation of cardiac myocytes cultured on scaffolds. Proc Natl Acad Sci U S A. 2004;101(52):18129–34.PubMedPubMedCentralGoogle Scholar
  68. 68.
    Maiullari F, Costantini M, Milan M, Pace V, Chirivì M, Maiullari S, et al. A multi-cellular 3D bioprinting approach for vascularized heart tissue engineering based on HUVECs and iPSC-derived cardiomyocytes. Sci Rep [Internet]. 2018 Dec [cited 2019 Feb 27];8(1). Available from:
  69. 69.
    •• Redd MA, Zeinstra N, Qin W, Wei W, Martinson A, Wang Y, et al. Patterned human microvascular grafts enable rapid vascularization and increase perfusion in infarcted rat hearts. Nat Commun. 2019;10(1):584. Current state-of-the-art showing vascular remodeling and integration of engineered microchannel networks. PubMedPubMedCentralGoogle Scholar
  70. 70.
    Zhang YS, Arneri A, Bersini S, Shin S-R, Zhu K, Goli-Malekabadi Z, et al. Bioprinting 3D microfibrous scaffolds for engineering endothelialized myocardium and heart-on-a-chip. Biomaterials. 2016;110:45–59.PubMedPubMedCentralGoogle Scholar
  71. 71.
    Miller JS, Stevens KR, Yang MT, Baker BM, Nguyen D-HT, Cohen DM, et al. Rapid casting of patterned vascular networks for perfusable engineered three-dimensional tissues. Nat Mater. 2012;11(9):768–74.PubMedPubMedCentralGoogle Scholar
  72. 72.
    Skylar-Scott MA, Gunasekaran S, Lewis JA. Laser-assisted direct ink writing of planar and 3D metal architectures. Proc Natl Acad Sci. 2016;113(22):6137–42.PubMedGoogle Scholar
  73. 73.
    Jang J, Park H-J, Kim S-W, Kim H, Park JY, Na SJ, et al. 3D printed complex tissue construct using stem cell-laden decellularized extracellular matrix bioinks for cardiac repair. Biomaterials. 2017;112:264–74.PubMedGoogle Scholar
  74. 74.
    Brandenberg N, Lutolf MP. In situ patterning of microfluidic networks in 3D cell-laden hydrogels. Adv Mater Deerfield Beach Fla. 2016;28(34):7450–6.Google Scholar
  75. 75.
    Brutsaert DL. Cardiac endothelial-myocardial signaling: its role in cardiac growth, contractile performance, and rhythmicity. Physiol Rev. 2003;83(1):59–115.PubMedGoogle Scholar
  76. 76.
    Montgomery M, Zhang B, Radisic M. Cardiac tissue vascularization: from angiogenesis to microfluidic blood vessels. J Cardiovasc Pharmacol Ther. 2014;19(4):382–93.PubMedGoogle Scholar
  77. 77.
    Potter RF, Groom AC. Capillary diameter and geometry in cardiac and skeletal muscle studied by means of corrosion casts. Microvasc Res. 1983;25(1):68–84.PubMedGoogle Scholar
  78. 78.
    Levenberg S, Rouwkema J, Macdonald M, Garfein ES, Kohane DS, Darland DC, et al. Engineering vascularized skeletal muscle tissue. Nat Biotechnol. 2005;23(7):879–84.PubMedGoogle Scholar
  79. 79.
    Tremblay P-L, Hudon V, Berthod F, Germain L, Auger FA. Inosculation of tissue-engineered capillaries with the host’s vasculature in a reconstructed skin transplanted on mice. Am J Transplant Off J Am Soc Transplant Am Soc Transpl Surg. 2005;5(5):1002–10.Google Scholar
  80. 80.
    Gulino D, Delachanal E, Concord E, Genoux Y, Morand B, Valiron MO, et al. Alteration of endothelial cell monolayer integrity triggers resynthesis of vascular endothelium cadherin. J Biol Chem. 1998;273(45):29786–93.PubMedGoogle Scholar
  81. 81.
    Schnaper HW, Kleinman HK. Regulation of cell function by extracellular matrix. Pediatr Nephrol Berl Ger. 1993;7(1):96–104.Google Scholar
  82. 82.
    Baiguera S, Ribatti D. Endothelialization approaches for viable engineered tissues. Angiogenesis. 2013;16(1):1–14.PubMedGoogle Scholar
  83. 83.
    Perry L, Flugelman MY, Levenberg S. Elderly patient-derived endothelial cells for vascularization of engineered muscle. Mol Ther J Am Soc Gene Ther. 2017;25(4):935–48.Google Scholar
  84. 84.
    Kurokawa YK, Yin RT, Shang MR, Shirure VS, Moya ML, George SC. Human induced pluripotent stem cell-derived endothelial cells for three-dimensional microphysiological systems. Tissue Eng Part C Methods. 2017;23(8):474–84.PubMedPubMedCentralGoogle Scholar
  85. 85.
    Kurisaki A, Ito Y, Onuma Y, Intoh A, Asashima M. In vitro organogenesis using multipotent cells. Hum Cell. 2010;23(1):1–14.PubMedGoogle Scholar
  86. 86.
    Elcheva I, Brok-Volchanskaya V, Kumar A, Liu P, Lee J-H, Tong L, et al. Direct induction of haematoendothelial programs in human pluripotent stem cells by transcriptional regulators. Nat Commun. 2014;5:4372.PubMedPubMedCentralGoogle Scholar
  87. 87.
    Chen X, Aledia AS, Ghajar CM, Griffith CK, Putnam AJ, Hughes CCW, et al. Prevascularization of a fibrin-based tissue construct accelerates the formation of functional anastomosis with host vasculature. Tissue Eng Part A. 2009;15(6):1363–71.PubMedGoogle Scholar
  88. 88.
    Hughes CCW. Endothelial-stromal interactions in angiogenesis. Curr Opin Hematol. 2008;15(3):204–9.PubMedPubMedCentralGoogle Scholar
  89. 89.
    Liu S, Zhang H, Zhang X, Lu W, Huang X, Xie H, et al. Synergistic angiogenesis promoting effects of extracellular matrix scaffolds and adipose-derived stem cells during wound repair. Tissue Eng Part A. 2011;17(5–6):725–39.PubMedGoogle Scholar
  90. 90.
    D’Amore PA. Capillary growth: a two-cell system. Semin Cancer Biol. 1992;3(2):49–56.PubMedGoogle Scholar
  91. 91.
    Ghajar CM, Chen X, Harris JW, Suresh V, Hughes CCW, Jeon NL, et al. The effect of matrix density on the regulation of 3-D capillary morphogenesis. Biophys J. 2008;94(5):1930–41.PubMedPubMedCentralGoogle Scholar
  92. 92.
    Velazquez OC, Snyder R, Liu Z-J, Fairman RM, Herlyn M. Fibroblast-dependent differentiation of human microvascular endothelial cells into capillary-like 3-dimensional networks. FASEB J Off Publ Fed Am Soc Exp Biol. 2002;16(10):1316–8.Google Scholar
  93. 93.
    Folkman J, D’Amore PA. Blood vessel formation: what is its molecular basis? Cell. 1996;87(7):1153–5.PubMedGoogle Scholar
  94. 94.
    Darland DC, D’Amore PA. Blood vessel maturation: vascular development comes of age. J Clin Invest. 1999;103(2):157–8.PubMedPubMedCentralGoogle Scholar
  95. 95.
    Darland DC, D’Amore PA. Cell-cell interactions in vascular development. Curr Top Dev Biol. 2001;52:107–49.PubMedGoogle Scholar
  96. 96.
    Arslan-Yildiz A, El Assal R, Chen P, Guven S, Inci F, Demirci U. Towards artificial tissue models: past, present, and future of 3D bioprinting. Biofabrication. 2016;8(1):014103.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Nazan Puluca
    • 1
    • 2
    • 3
    • 4
  • Soah Lee
    • 1
    • 4
  • Stefanie Doppler
    • 2
    • 3
  • Andrea Münsterer
    • 2
    • 3
  • Martina Dreßen
    • 2
    • 3
  • Markus Krane
    • 2
    • 3
    • 5
  • Sean M. Wu
    • 1
    • 4
    Email author
  1. 1.Division of Cardiovascular Medicine, Department of Medicine; Institute of Stem Cell Biology and Regenerative MedicineStanford University School of MedicineStanfordUSA
  2. 2.Department of Cardiovascular Surgery, German Heart Center MunichTechnische Universität MünchenMunichGermany
  3. 3.Insure (Institute for Translational Cardiac Surgery) Department of Cardiovascular Surgery, German Heart Center MunichTechnische Universität MünchenMunichGermany
  4. 4.Cardiovascular InstituteStanford University School of MedicineStanfordUSA
  5. 5.German Heart Center Munich-DZHK Partner Site Munich Heart AllianceMunichGermany

Personalised recommendations